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Investigations on Mechanisms of Survival and Pathogenesis of Mycobacterium Ulcerans in Polymicrobial Environments

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Investigations on Mechanisms of Survival and Pathogenesis of Mycobacterium Ulcerans in Polymicrobial Environments Mississippi State University Scholars Junction Theses and Dissertations Theses and Dissertations 11-25-2020 Investigations on mechanisms of survival and pathogenesis of Mycobacterium ulcerans in polymicrobial environments Laxmi Dhungel Follow this and additional works at: https://scholarsjunction.msstate.edu/td Recommended Citation Dhungel, Laxmi, "Investigations on mechanisms of survival and pathogenesis of Mycobacterium ulcerans in polymicrobial environments" (2020). Theses and Dissertations. 2872. https://scholarsjunction.msstate.edu/td/2872 This Dissertation - Open Access is brought to you for free and open access by the Theses and Dissertations at Scholars Junction. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of Scholars Junction. For more information, please contact [email protected]. Template C with Schemes v4.1 (beta): Created by L. Threet 11/15/19 Investigations on mechanisms of survival and pathogenesis of Mycobacterium ulcerans in polymicrobial environments By TITLE PAGE Laxmi Dhungel Approved by: Heather Jordan (Major Professor) Mark Eric Benbow Keun Seok Seo Justin A. Thornton (Graduate Coordinator) Rick Travis (Dean, College of Arts & Sciences) A Dissertation Submitted to the Faculty of Mississippi State University in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Microbiology in the Department of Biological Sciences Mississippi State, Mississippi November 2020 Copyright by COPYRIGHT PAGE Laxmi Dhungel 2020 Name: Laxmi Dhungel ABSTRACT Date of Degree: November 25, 2020 Institution: Mississippi State University Major Field: Microbiology Major Professor: Heather Jordan Title of Study: Investigations on mechanisms of survival and pathogenesis of Mycobacterium ulcerans in polymicrobial environments Pages in Study: 274 Candidate for Degree of Doctor of Philosophy Buruli ulcer disease (BUD) remains a ‘mysterious disease’ due to the unknown mode of M. ulcerans transmission and pathogenesis. To understand these, it is important to determine the reservoir of the organism in its natural environments, and stress response and interactions of M. ulcerans in its natural niche and during infection of a host. The major virulence factor of M. ulcerans is mycolactone, a lipid cytotoxin that is encoded on a giant plasmid pMUM001. Genetic analysis suggests that plasmid pMUM001 was acquired by M. ulcerans during evolution from its progenitor, M. marinum. Coincidental evolution of virulence hypothesis suggests that many microbes evolve to acquire traits to outcompete or overcome biotic and abiotic forces during their normal life cycle in the outside-host environment, which can confer virulence during infection of a human host. Hence in this study, we exposed M. ulcerans to selective abiotic forces such as UV, and dynamic oxygen and temperature conditions to determine their effect on M. ulcerans growth, and mycolactone and global gene expression. We also studied the role of mycolactone in determining polymicrobial interaction of M. ulcerans in its natural aquatic habitat by exposing mycolactone coated and uncoated slides in M. ulcerans endemic and non-endemic aquatic locations and determining differences in microbial community composition between them. Further, we studied quorum quenching ability of mycolactone against an opportunistic pathogen, S. aureus. The results obtained showed that exposure of M. ulcerans to abiotic stresses such as higher temperature and lower than optimal oxygen conditions modulate its global and mycolactone gene expression. Further, we also showed that mycolactone can impact overall microbial community structure in a polymicrobial environment in its natural, aquatic habitat. Mycolactone also effected virulence and quorum sensing in an opportunistic pathogen, S. aureus, without inhibiting its growth. These findings are important as they provide insight toward potential reservoirs or environmental niches which may harbor M. ulcerans and inform new potential mechanisms of pathogenesis. Further, our novel research of synergistic or antagonistic interactions within the complex polymicrobial communities colonizing skin and aquatic habitats is a powerful approach in determining M. ulcerans colonization efficiency, resiliency, and transmission mechanisms. DEDICATION I would like to dedicate this dissertation to my loving husband Dr. Durga Prasad Siwakoti and son Dibesh Siwakoti who have been and remain my guidance, support, and inspiration. To be loved by you makes me feel one of the luckiest in the world. I would also want to dedicate this to my father Khagendra Prasad Dhungel and mother Januka Devi Dhungel for their love and motivation. I am thankful to them for educating me and making me capable of pursuing my dream. I would also like to dedicate this work to my brothers Arjun Kumar Dhungel and Krishna Prasad Dhungel for being with me during my highs and lows. ii ACKNOWLEDGEMENTS I am extremely thankful to my mentor, Dr. Heather Jordan for providing continuous guidance and support throughout my Ph. D journey. This work would have been impossible without her. I am glad that she believed me as a researcher and answered all the questions, even though they sound stupid sometimes. Thank you for encouraging and instilling scientist on me. Thank you for all the nomination and recommendation letters. I am proud and fortunate to be your student. I would also like to thank my committee members Dr. Eric Benbow, Dr. Keun Seok Seo and Dr. Justin Thornton for their contributions in my projects. The work, constructive comments, and suggestions you all provided are the backbone of this dissertation. Thank you for providing your valuable time in completion of this project. I would like to thank my lab mates Dr. Zach Burcham, Dr. Jonathan Belanich, Emilia Kooienga and Lindsay Harrison for their cooperation and being amazing lab mates. I would like to thank Dr. Lindsey Burcham for conducting experiment on “Effect of mycolactone on S. aureus growth”. I also want to thank my undergraduate students Raisa Bonner, Albert Codjue, Meagan Cook, Duncan Henson, Alexis Lewis, Trent Moulder, Kelton Reynolds and Harshini Devi iii Sampathkumar for their invaluable work. It was a great teaching and learning experience for me as well. I am proud of mentoring you all. I would also like to thank Graduate Coordinator Dr. Justin Thornton and Head of Department Dr. Angus Dawe for providing academic guidance during my years in the department. I would also like to thank Ms. Rita Christopher, Ms. Rhonda Hannah, Ms. Denice Miller, Ms. Mari Shurden and Ms. Martha Wilson for all the administrative works in Department of Biological Sciences, Mississippi State University. I would like to thank my TA lab instructors Mr. Jeffery Echols, Mr. Tom Holder, Dr. Victoria McCurdy, Dr. Brandy Roberts, and Ms. Gay Williamson for their guidance and support during my journey as a teaching assistant. I am grateful to all Mississippi State University family for this opportunity and love. iv TABLE OF CONTENTS DEDICATION ................................................................................................................................ ii ACKNOWLEDGEMENTS ........................................................................................................... iii LIST OF TABLES ...........................................................................................................................x LIST OF FIGURES ....................................................................................................................... xi CHAPTER I. LINKING THE MYCOBACTERIUM ULCERANS ENVIRONMENT TO BURULI ULCER DISEASE: PROGRESS AND CHALLENGES (INTRODUCTION) ..............1 1.1 Abstract ..................................................................................................................1 1.2 Introduction ...........................................................................................................2 1.3 Epidemiology of the disease ..................................................................................3 1.4 Clinical presentation of BUD ................................................................................6 1.5 BUD in immunocompromised individuals and BUD complications ....................8 1.6 Diagnosis, prevention and treatment of the disease ............................................10 1.7 Socio-cultural, psychological and economic impact of the disease ....................12 1.8 Microbiology of Buruli ulcer disease ..................................................................14 1.9 Pathogenicity and virulence ................................................................................16 1.10 The ecology of M. ulcerans .................................................................................20 1.10.1 Detection of M. ulcerans in the environment ................................................21 1.10.2 Presence of M. ulcerans in aquatic environmental samples ..........................22 1.10.3 M. ulcerans in non-mosquito aquatic invertebrates ......................................23 1.10.4 M. ulcerans in mosquitoes .............................................................................25 1.10.5 M. ulcerans in mammals ...............................................................................26 1.10.6 M. ulcerans detected in other sources ...........................................................27 1.11 Hypothesized modes of transmission ..................................................................28
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